This article requires a subscription to view the full text. If you have a subscription you may use the login form below to view the article. Access to this article can also be purchased.

Significance

Cell communities can become resilient to stress by undergoing collective growth oscillations, which provide periodic stress relief and are collective in the sense that they arise only for large enough numbers of cells. Collective oscillatory phenomena usually emerge continuously as the system size increases, with oscillations starting with small amplitude and slowly growing as the cells proliferate. This behavior, however, is not appropriate in situations in which the population needs to implement a full-sized response quickly. Our combined theoretical and experimental study shows that collective oscillations in bacterial biofilm communities emerge via a discontinuous transition as their size increases. This behavior may provide an evolutionary advantage to cell communities, by allowing them to quickly alter qualitatively their dynamics in response to variations in external conditions such as stress.

Abstract

Biofilm communities of Bacillus subtilis bacteria have recently been shown to exhibit collective growth-rate oscillations mediated by electrochemical signaling to cope with nutrient starvation. These oscillations emerge once the colony reaches a large enough number of cells. However, it remains unclear whether the amplitude of the oscillations, and thus their effectiveness, builds up over time gradually or if they can emerge instantly with a nonzero amplitude. Here we address this question by combining microfluidics-based time-lapse microscopy experiments with a minimal theoretical description of the system in the form of a delay-differential equation model. Analytical and numerical methods reveal that oscillations arise through a subcritical Hopf bifurcation, which enables instant high-amplitude oscillations. Consequently, the model predicts a bistable regime where an oscillating and a nonoscillating attractor coexist in phase space. We experimentally validate this prediction by showing that oscillations can be triggered by perturbing the media conditions, provided the biofilm size lies within an appropriate range. The model also predicts that the minimum size at which oscillations start decreases with stress, a fact that we also verify experimentally. Taken together, our results show that collective oscillations in cell populations can emerge suddenly with nonzero amplitude via a discontinuous transition.

Blood-sucking sand flies from disparate global regions have a predilection for feeding on the marijuana plant (Cannabis sativa), and the findings hint at a potential avenue for controlling sand flies, which can transmit leishmaniasis.